The Role of the Extrafibrillar Volume on the Mechanical Properties of Molecular Models of Mineralized Bone Microfibrils.

Bones are responsible for body support, structure, motion, and several other functions that enable and facilitate life for many different animal species. They exhibit a complex network of distinct physical structures and mechanical properties, which ultimately depend on the fraction of their primary constituents at the molecular scale. However, the relationship between structure and mechanical properties in bones are still not fully understood. Here, we investigate structural and mechanical properties of all-atom bone molecular models composed of type-I collagen, hydroxyapatite (HA), and water by means of fully atomistic molecular dynamics simulations. Our models encompass an extrafibrillar volume (EFV) and consider mineral content in both the EFV and intrafibrillar volume (IFV), consistent with experimental observations. We investigate solvation structures and elastic properties of bone microfibril models with different degrees of mineralization, ranging from highly mineralized to weakly mineralized and nonmineralized models. We find that the local tetrahedral order of water is lost in similar ways in the EFV and IFV regions for all HA containing models, as calcium and phosphate ions are strongly coordinated with water molecules. We also subject our models to tensile loads and analyze the spatial stress distribution over the nanostructure of the material. Our results show that both mineral and water contents accumulate significantly higher stress levels, most notably in the EFV, thus revealing that this region, which has been only recently incorporated in all-atom molecular models, is fundamental for studying the mechanical properties of bones at the nanoscale. Furthermore, our results corroborate the well-established finding that high mineral content makes bone stiffer.